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(Malvaceae) in the Mascarenes: Old Taxa on Young Islands?

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(Malvaceae) in the Mascarenes: Old Taxa on Young Islands? Int. J. Plant Sci. 176(3):211–221. 2015. q 2015 by The University of Chicago. All rights reserved. 1058-5893/2015/17603-0001$15.00 DOI:10.1086/679350 DIVERSIFICATION OF DOMBEYOIDEAE (MALVACEAE) IN THE MASCARENES: OLD TAXA ON YOUNG ISLANDS? Timothée Le Péchon,1,*,† Qiang Dai,* Li-Bing Zhang,*,‡ Xin-Fen Gao,* and Hervé Sauquet§ *Chengdu Institute of Biology, Chinese Academy of Sciences, PO Box 416, Chengdu, Sichuan 610041, China; †Université de La Réunion, Laboratoire d’Informatique et Mathématiques–Institut de Recherche en Mathématiques et Informatique Appliquées, 2 Rue Joseph Wetzell, Bat. 2, F-97490 Sainte-Clotilde, La Réunion, France; ‡Missouri Botanical Garden, PO Box 299, St. Louis, Missouri 63166-0299, USA; and §Laboratoire Ecologie, Systématique, Evolution, Université Paris-Sud, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 8079, 91405 Orsay, France Editor: Félix Forest Premise of research. The patterns of diversification of Mascarene taxa remain largely unknown in com- parison to other insular systems. Traditional interpretations of insular radiations often assume that endemic taxa radiated after the origin of the insular habitats on which they were established. The Dombeyoideae (Malvaceae) sublineage endemic to Mauritius and Réunion in the Mascarenes is an ideal model to test for the signature of insular diversification. Methodology. We combined molecular sequences for a dense sample of Mascarene dombeyoids together with African, Malagasy, and Asian outgroup species. We estimated divergence times based on two calibration schemes (including or excluding geological calibration). Comparative phylogenetic methods were used to study the diversification rates and the evolution of the floral disparity in the Mascarene clade. Pivotal results. Excluding geological constraints resulted in drastically older age estimates than when we included such calibrations. Diversification patterns suggest a decrease of diversification rates through time. The low morphological disparity indicates an early partitioning of floral characters. Conclusions. The lineage diversification and the morphological disparity are consistent with traditional scenarios of insular radiation. However, the Mascarene clade is older than Réunion and Mauritius, suggesting the onset of radiation before the formation of the archipelago. The diversification might have been driven by geographical opportunity rather than ecological opportunity. Keywords: Dombeya, island radiation, lineage diversification, morphological disparity, the Mascarenes, Trochetia. Online enhancements: appendix figures and tables. Introduction the activity of the Madagascar and Indian Ocean islands bio- diversity hot spot. The largest island, Réunion, possesses an Due to their similar properties (e.g., small size, isolation from active volcano and a high mountainous formation, with its the continental landmass, and distinct boundaries), oceanic is- highest peak at 3070 m. Although older and lower than Ré- lands and similar isolated habitats (such as lakes or caves) are union, Mauritius also presents a high diversity of isolated considered attractive environments for studying patterns and habitats because of the natural erosion and recent lava flows processes driving species diversification (Carlquist 1974; Giv- that have deeply modified the island (McDougall and Cha- nish 1997; Emerson 2002). The Mascarene Archipelago con- malaun 1969). As a consequence, both islands show dra- sists of three young oceanic islands (Réunion [2–5 Ma], matic topographical contrasts, and this heterogeneity has led Mauritius [8–10 Ma], and Rodrigues [8–10 Ma]; McDougall to the formation of numerous and diverse habitats (Thébaud et al. 1965; McDougall and Chamalaun 1969; Sheth et al. et al. 2009). As in many other oceanic archipelagos, the 2003) that (with the exception of Rodrigues) originated from Mascarene biota is characterized by high levels of endemism and a relatively low number of species compared with similar habitats in mainland regions (Thébaud et al. 2009). Despite 1 Author for correspondence; current address: School of Life Sci- showing interesting features for the study of evolutionary ences, University of KwaZulu-Natal, Private Bag X01, Scottsville, processes, the biogeography and patterns of diversification of Pietermaritzburg 3209, South Africa; e-mail: [email protected]. Mascarene taxa remain largely unknown in comparison to Manuscript received July 2014; revised manuscript received September 2014; other insular systems such as Hawaii or the Galapagos (Parent electronically published January 21, 2015. et al. 2008; Baldwin and Wagner 2010). Although the number 211 212 INTERNATIONAL JOURNAL OF PLANT SCIENCES of available phylogenetic studies of Mascarene taxa has in- Subfamily Dombeyoideae (Malvaceae s.l., cotton family) creased over the last few years (e.g., Maurin et al. 2007; includes ca. 350 plant species distributed in the Paleotropical Micheneau et al. 2008), only a handful of these studies (e.g., region, with the highest diversity found in Madagascar and Harmon et al. 2008a; Strijk et al. 2012, 2014) have analyzed neighboring islands (ca. 250 species; Kubitzki and Bayer diversification in light of the new framework of tests and 2003). The 24 dombeyoid species present in the Mascarenes, methodological tools now available (Rabosky 2006b; Harmon of which 23 (96%) are endemic, represent emblematic com- et al. 2008b; Glor 2010; Stadler 2011). ponents of the Mascarene biotas (Cadet 1980; Thébaud et al. In such modern approaches, the estimate of a temporal phy- 2009). Two recent phylogenetic investigations showed that logenetic framework has a central place for studying diversifi- the Dombeyoideae of the Mascarenes are polyphyletic and dis- cation patterns. The most common practice is to use temporal tributed in four clades (Le Péchon et al. 2010; Skema 2012). constraints provided by fossil records as a source of node cal- However, both studies have identified one particular well- ibration for relaxed clock molecular dating analyses (Ho and supported clade (hereafter, clade A) endemic to the archipelago Phillips 2009; Sauquet et al. 2012). However, for taxa with a (Mauritius and Réunion). This clade includes 11 species be- poor fossil record, using geological calibrations as a maximum longing to three genera: Dombeya Cav. (4 spp.; fig. 1A,1E), age bound is an occasional practice in molecular dating anal- Ruizia Cav. (1 species; fig. 1B), and Trochetia DC. (6 spp.; yses, particularly in groups that have diversified on oceanic is- fig. 1C,1D,1F). Dombeya includes many more species outside lands (e.g., Austin et al. 2004). This approach has been widely this clade and is known to be paraphyletic as a whole, but criticized, mainly because of the implicit assumption that di- phylogenetic analyses have consistently shown that the re- vergence events do not predate island ages, that is, the hy- maining species branch outside this Mascarene clade (Le pothesis that the endemic clade must have diversified in situ Péchon et al. 2010, 2013a; Skema 2012). The species in clade (Emerson 2007; Forest 2009; Heads 2011). This critical as- A also show a wide range of variation in floral, anatomical, sumption is not always verified, and using hard constraints vegetative, and reproductive characters (Friedmann 1987; Hu- based on island age may strongly impact divergence time esti- meau et al. 1999; Le Péchon et al. 2009, 2011a, 2011b; Boura mates, but very few studies have tested this impact so far (e.g., et al. 2011). Therefore, clade A represents an interesting op- Mello and Schrago 2012). portunity to test for and characterize a possible insular radia- Fig. 1 Morphological diversity of Mascarene dombeyoids (clade A, endemic to Mauritius and Réunion). A, Dombeya populnea. B, Tro- chetia blackburniana. C, Trochetia parviflora. D, Ruizia cordata. E, Dombeya ferruginea subsp. borbonica. F, Trochetia granulata. Photographs by David Caron (A, D, E, F) and Timothée Le Péchon (B, C), BACOMAR project. LE PÉCHON ET AL.—ENDEMIC RADIATION IN THE MASCARENE DOMBEYOIDEAE 213 tion using recently developed methods for studying diversifi- Phylogenetic relationships were reconstructed using maxi- cation. In this study, we reconstruct the first time-calibrated mum likelihood (ML) and Bayesian inference (BI) on the com- phylogenetic framework for Dombeyoideae using two different bined data set. Maximum likelihood analyses were performed calibration schemes to estimate the impact of calibrations on with RAxML 7.3.5 (Stamatakis 2006), with each molecular age estimates. By using geological calibrations in one of these region assigned a separate partition using the GTRGAMMA two schemes, we aim to evaluate the impact of such practice on model of sequence evolution. The best-known likelihood tree the inference of the diversification process. From the resulting was found using default search parameters and 100 search chronograms, we examine the pattern of lineage proliferation replicates. Node support was estimated using a bootstrap (BS) and morphological disparification in clade A. We then compare analysis with 1000 replicates. Bayesian inference analyses the diversification pattern of clade A with radiations of island- were conducted using MrBayes, version 3.1.2 (Ronquist and endemic taxa and discuss the possible evolutionary processes Huelsenbeck 2003), with each DNA region treated as a separate that may have driven its diversification. partition, and run on the CIPRES cluster (Miller et al. 2010). Four chains of Metropolis-coupled Markov chain
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